Abstract

We report here that a meiosis-specific gene of Schizosaccharomyces pombe denoted mcp6+ (meiotic coiled-coil protein) encodes a protein that is required for the horsetail movement of chromosomes at meiosis I. The mcp6+ gene is specifically transcribed during the horsetail phase. Green fluorescent protein (GFP)-tagged Mcp6 appears at the start of karyogamy, localizes to the spindle-pole body (SPB) and then disappears before chromosome segregation at meiosis I. In the mcp6Delta strain, the horsetail movement was either hampered (zygotic meiosis) or abolished (azygotic meiosis) and the pairing of homologous chromosomes was impaired. Accordingly, the allelic recombination rates of the mcp6Delta strain were only 10-40% of the wild-type rates. By contrast, the ectopic recombination rate of the mcp6Delta strain was twice the wild-type rate. This is probably caused by abnormal homologous pairing in mcp6Delta cells because of aberrant horsetail movement. Fluorescent microscopy indicates that SPB components such as Sad1, Kms1 and Spo15 localize normally in mcp6Delta cells. Because Taz1 and Swi6 also localized with Sad1 in mcp6Delta cells, Mcp6 is not required for telomere clustering. In a taz1Delta strain, which does not display telomere clustering, and the dhc1-d3 mutant, which lacks horsetail movement, Mcp6 localized with Sad1 normally. However, we observed abnormal astral microtubule organization in mcp6Delta cells. From these results, we conclude that Mcp6 is necessary for neither SPB organization nor telomere clustering, but is required for proper astral microtubule positioning to maintain horsetail movement.

Highlights

  • Reproducing eukaryotic organisms undergo meiosis, a special type of cell division, to generate inheritable haploid gametes from diploid parental cells

  • In mcp6∆ cells, there was no significant difference from the wild type in the initial 45 minutes but the subsequent increase in pairing observed in the wild type was completely absent (Fig. 4B, red line). These results indicate that Mcp6 is required for promoting homologous pairing with horsetail movement

  • The Swi6-Green fluorescent protein (GFP) signal localized with the Sad1-DsRed signal to the spindle-pole body (SPB) at similar levels in mcp6∆ (76%; 13/17) and wild-type cells (85%; 35/41) (Fig. 8B). These results indicate that the subcellular localization of Taz1 and Swi6 is normal in mcp6∆ cells – namely, Mcp6 is required for neither SPB organization nor telomere clustering

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Summary

Introduction

Reproducing eukaryotic organisms undergo meiosis, a special type of cell division, to generate inheritable haploid gametes from diploid parental cells. This process includes meiosis-specific events that increase genetic diversity, such as synaptonemal complex (SC) formation, homologous pairing and recombination. An essential event for efficient chromosome pairing in S. pombe is the clustering during prophase of meiosis I of the telomeres of three chromosomes near the spindle-pole body (SPB) (Chikashige et al, 1994; Chikashige et al, 1997) This characteristic arrangement of meiotic chromosomes has been observed in a wide range of organisms and is denoted a ‘bouquet’ arrangement (Loidl, 1990; Scherthan, 2001; Zickler and Kleckner, 1999). This arrangement has been proposed to facilitate homologous chromosome pairing because it generates a polarized chromosome configuration by bundling chromosomes together at their telomeres

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